Skip to main content
SpringerLink
Log in

Surgery for Hepatocellular Carcinoma in Patients with Child–Pugh B Cirrhosis: Hepatic Resection Versus Living Donor Liver Transplantation

  • Original Scientific Report
  • Published:
World Journal of Surgery Aims and scope Submit manuscript

Abstract

Background

Liver transplantation has been established as the optimal treatment for hepatocellular carcinoma in cirrhotic patients, but hepatic resection is also effective in patients with well-preserved liver function. Determining the suitable surgical treatment for patients with Child–Pugh class B cirrhosis is a more difficult challenge.

Methods

We retrospectively compared the results of hepatic resection and living donor liver transplantation for hepatocellular carcinoma in 137 patients with Child–Pugh class B cirrhosis. The procedures were performed at Kyushu University Hospital from April 2014 through October 2016.

Results

Patients who underwent hepatic resection were significantly older and had better liver function, larger tumor size, smaller number of tumors, and less surgical stress compared with patients who underwent living donor liver transplantation. The overall survival rate and the recurrence-free survival rate in patients with transplantation were significantly better than that in patients with resection. The multivariate analysis showed that recurrent hepatocellular carcinoma and microvascular invasion were significant prognostic factors for both overall and recurrence-free survival in the hepatic resection group. In the group with protein induced by vitamin K absence or antagonist-II ≥300 mAU/mL, both the overall survival curve and the recurrence-free survival curve in patients with living donor liver transplantation were not significantly different from those in patients with hepatic resection.

Conclusions

Living donor liver transplantation for hepatocellular carcinoma in patients with Child–Pugh class B cirrhosis was favorable under the condition of protein induced by vitamin K absence or antagonist-II <300 mAU/mL in selected recipients and donors. Hepatic resection for recurrent hepatocellular carcinoma and excessive blood loss should be avoided in patients with Child–Pugh class B cirrhosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

GV/SLV:

Graft volume/standard liver volume ratio

HCC:

Hepatocellular carcinoma

HR:

Hepatic resection

LDLT:

Living donor liver transplantation

LT:

Liver transplantation

PIVKA-II:

Protein induced by vitamin K absence or antagonist-II

PV:

Portal vein

References

  1. Llovcet JM, Burroughs A, Bruix J (2003) Hepatocellular carcinoma. Lancet 362:1907–1917

    Article  Google Scholar 

  2. Kiyosawa K, Tanaka E (2002) Characteristics of hepatocellular carcinoma in Japan. Oncology 62:5–7

    Article  PubMed  Google Scholar 

  3. Shimada M, Takenaka K, Taguchi K, Fujiwara Y, Gion T, Kajiyama K et al (1998) Prognostic factors after repeat hepatectomy for recurrent hepatocellular carcinoma. Ann Surg 227(1):80–85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Shimada M, Takenaka K, Gion T, Fujiwara Y, Kajiyama K, Maeda T et al (1996) Prognosis of recurrent hepatocellular carcinoma: a 10-year surgical experience in Japan. Gastroenterology 111(3):720–726

    Article  PubMed  CAS  Google Scholar 

  5. Minagawa M, Makuuchi M, Takayama T, Kokudo N (2003) Selection criteria for repeat hepatectomy in patients with recurrent hepatocellular carcinoma. Ann Surg 238(5):703–710

    Article  PubMed  PubMed Central  Google Scholar 

  6. Itamoto T, Nakahara H, Amano H, Kohashi T, Ohdan H, Tashiro H et al (2007) Repeat hepatectomy for recurrent hepatocellular carcinoma. Surgery 141(5):589–597

    Article  PubMed  Google Scholar 

  7. Mazzaferro V, Regalia E, Doci R, Andreola S, Pulvirenti A, Bozzetti F et al (1996) Liver transplantation for the treatment of small hepatocellular carcinomas in patients with cirrhosis. N Engl J Med 334(11):693–699

    Article  PubMed  CAS  Google Scholar 

  8. Llovet JM, Bruix J, Gores GJ (2000) Surgical resection versus transplantation for early hepatocellular carcinoma: clues for the best strategy. Hepatology 31(4):1019–1021

    Article  PubMed  CAS  Google Scholar 

  9. Bruix J, Llovet JM (2002) Prognostic prediction and treatment strategy in hepatocellular carcinoma. Hepatology 35(3):519–524

    Article  PubMed  Google Scholar 

  10. Bismuth H, Chiche L, Adam R, Castaing D, Diamond T, Dennison A (1993) Liver resection versus transplantation for hepatocellular carcinoma in cirrhotic patients. Ann Surg 218(2):145–151

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Sarasin FP, Giostra E, Mentha G, Hadengue A (1998) Partial hepatectomy or orthotopic liver transplantation for the treatment of resectable hepatocellular carcinoma? A cost-effectiveness perspective. Hepatology 28(2):436–442

    Article  PubMed  CAS  Google Scholar 

  12. Michel J, Suc B, Montpeyroux F, Hachemanne S, Hachemanne S, Blanc P, Domergue J et al (1997) Liver resection or transplantation for hepatocellular carcinoma? Retrospective analysis of 215 patients with cirrhosis. J Hepatol 26(6):1274–1280

    Article  PubMed  CAS  Google Scholar 

  13. Jiang L, Liao A, Wen T, Yan L, Li B, Yang J (2014) Living donor liver transplantation or resection for Child-Pugh A hepatocellular carcinoma patients with multiple nodules meeting the Milan criteria. Transplant Int 27(6):562–569

    Article  Google Scholar 

  14. Chan AC, Chan SC, Chok KS, Cheung TT, Chiu DW, Poon RT et al (2013) Treatment strategy for recurrent hepatocellular carcinoma: salvage transplantation, repeated resection, or radiofrequency ablation? Liver Transplant 19(4):411–419

    Article  Google Scholar 

  15. Shen JY, Li C, Wen TF et al (2016) Liver transplantation versus surgical resection for HCC meeting the Milan criteria: a propensity score analysis. Medicine 95(52):e5756

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240(2):205–213

    Article  PubMed  PubMed Central  Google Scholar 

  17. Yonemura Y, Taketomi A, Soejima Y, Yoshizumi T, Uchiyama H, Gion T et al (2005) Validity of preoperative volumetric analysis of congestion volume in living donor liver transplantation using three-dimensional computed tomography. Liver Transplant 11(12):1556–1562

    Article  Google Scholar 

  18. Yamashita Y, Taketomi A, Itoh S, Kitagawa D, Kayashima H, Harimoto N et al (2007) Longterm favorable results of limited hepatic resections for patients with hepatocellular carcinoma: 20 years of experience. J Am Coll Surg 205(1):19–26

    Article  PubMed  Google Scholar 

  19. Rahbari NN, Koch M, Mehabi A, Weidmann K, Motschall E, Kahlert C et al (2009) Portal triad clamping versus vascular exclusion for vascular control during hepatic resection: a systematic review and meta-analysis. J Gastrointest Surg 13:558–568

    Article  PubMed  Google Scholar 

  20. Taketomi A, Morita K, Toshima T, Takeishi K, Kayashima H, Ninomiya M et al (2010) Living donor hepatectomies with procedures to prevent biliary complications. J Am Coll Surg 211:456–464

    Article  PubMed  Google Scholar 

  21. Liver cancer study group of Japan (2003) General rules for the clinical and pathological study of primary liver cancer, second English edition. Kanehara & Co., Tokyo, pp 34–35

  22. Mazzaferro V, Llovet JM, Miceli R, Bhoori S, Schiavo M, Mariani L, Metroticket Investigator Study Group et al (2009) Predicting survival after liver transplantation in patients with hepatocellular carcinoma beyond the Milan criteria: a retrospective, exploratory analysis. Lancet Oncol 10(1):35–43

    Article  PubMed  Google Scholar 

  23. Taketomi A, Sanefuji K, Soejima Y, Yoshizumi T, Uhciyama H, Ikegami T et al (2009) Impact of des-gamma-carboxy prothrombin and tumor size on the recurrence of hepatocellular carcinoma after living donor liver transplantation. Transplantation 87(4):531–537

    Article  PubMed  Google Scholar 

  24. Harimoto N, Shirabe K, Nakagawara H, Toshima T, Yamashita Y, Ikegami T et al (2013) Prognostic factors affecting survival at recurrence of hepatocellular carcinoma after living-donor liver transplantation: with special reference to neutrophil/lymphocyte ratio. Transplantation 96(11):1008–1012

    Article  PubMed  CAS  Google Scholar 

  25. Motomura T, Shirabe K, Mano Y, Muto J, Toshima T, Umemoto Y et al (2013) Neutrophil-lymphocyte ratio reflects hepatocellular carcinoma recurrence after liver transplantation via inflammatory microenvironment. J Hepatol 58(1):58–64

    Article  PubMed  CAS  Google Scholar 

  26. Escartin A, Sapisochin G, Bilbao I, Vilallonga R, Bueno J, Castells L et al (2007) Recurrence of hepatocellular carcinoma after liver transplantation. Transplant Proc 39:2308–2310

    Article  PubMed  CAS  Google Scholar 

  27. Regalia E, Fassati LR, Valente U, Pulvirenti A, Damilano I, Dardano G et al (1998) Pattern and management of recurrent hepatocellular carcinoma after liver transplantation. J Hepatobiliary Pancreat Surg 5:29–34

    Article  PubMed  CAS  Google Scholar 

  28. Shin WY, Suh KS, Lee HW, Kim J, Kim T, Yi NJ et al (2010) Prognostic factors affecting survival after recurrence in adult living donor liver transplantation for hepatocellular carcinoma. Liver Transplant 16(5):678–684

    Article  Google Scholar 

  29. Taketomi A, Fukuhara T, Morita K, Kayashima H, Ninomiya M, Yamashita Y et al (2010) Improved results of a surgical resection for the recurrence of hepatocellular carcinoma after living donor liver transplantation. Ann Surg Oncol 17(9):2283–2289

    Article  PubMed  Google Scholar 

  30. Roayaie S, Schwartz JD, Sung MW, Emre SH, Miller CM, Gondolesi GE et al (2004) Recurrence of hepatocellular carcinoma after liver transplant: patterns and prognosis. Liver Transplant 10:534–540

    Article  Google Scholar 

  31. Schlitt HJ, Neipp M, Weimann A, Oldhafer KJ, Schmoll E, Boeker K et al (1999) Recurrence patterns of hepatocellular and fibrolamellar carcinoma after liver transplantation. J Clin Oncol 17(1):324–331

    Article  PubMed  CAS  Google Scholar 

  32. Yokoyama I, Carr B, Saitsu H, Iwatsuki S, Starzl TE (1991) Accelerated growth rates of recurrent hepatocellular carcinoma after liver transplantation. Cancer 68(10):2095–2100

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Yoshizumi T, Ikegami T, Bekki Y, Ninomiya M, Uchiyama H, Iguchi T et al (2014) Re-evaluation of the predictive score for 6-month graft survival in living donor liver transplantation in the modern era. Liver Transplant 20(3):323–332

    Article  Google Scholar 

  34. Ikegami T, Shirabe K, Yoshiya S, Yoshizumi T, Ninomiya M, Uchiyama H et al (2012) Bacterial sepsis after living donor liver transplantation: the impact of early enteral nutrition. J Am Coll Surg 214(3):288–295

    Article  PubMed  Google Scholar 

  35. Harimoto N, Yoshida Y, Kurihara T, Takeishi K, Itoh S, Harada N et al (2015) Prognostic impact of des-γ-carboxyl prothrombin in living-donor liver transplantation for recurrent hepatocellular carcinoma. Transplant Proc 47(3):703–704

    Article  PubMed  CAS  Google Scholar 

  36. Nagasue N, Yukaya H, Ogawa Y, Sasaki Y, Chang YC, Niimi K (1986) Second hepatic resection for recurrent hepatocellular carcinoma. Br J Surg 73(6):434–438

    Article  PubMed  CAS  Google Scholar 

  37. Yamashita Y, Yoshida Y, Kurihara T, Itoh S, Harimoto N, Ikegami T, Yoshizumi T et al (2015) Surgical results for recurrent hepatocellular carcinoma after curative hepatectomy: repeat hepatectomy versus salvage living donor liver transplantation. Liver Transplant 21(7):961–968

    Article  Google Scholar 

  38. Harada N, Shirabe K, Ikeda Y, Korenaga D, Takenaka K, Maehara Y (2012) Surgical management of hepatocellular carcinoma in Child-Pugh class B cirrhotic patients: hepatic resection and/or microwave coagulation therapy versus living donor liver transplantation. Ann Transplant 17(4):11–20

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Andrea Baird, MD, from Edanz Group (www.edanzediting.com/ac) for editing a draft of this manuscript.

Author information

Authors and Affiliations

  1. Department of Surgery and Science, Graduate School of Medical Sciences, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka, 812-8582, Japan

    Norifumi Harimoto, Tomoharu Yoshizumi, Yukiko Fujimoto, Takashi Motomura, Youhei Mano, Takeo Toshima, Shinji Itoh, Noboru Harada, Toru Ikegami, Hideaki Uchiyama, Yuji Soejima & Yoshihiko Maehara

Authors
  1. Norifumi Harimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tomoharu Yoshizumi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yukiko Fujimoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Takashi Motomura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Youhei Mano
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Takeo Toshima
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shinji Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Noboru Harada
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Toru Ikegami
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Hideaki Uchiyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Yuji Soejima
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yoshihiko Maehara
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Norifumi Harimoto.

Ethics declarations

Conflict of interest

All authors declare no conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harimoto, N., Yoshizumi, T., Fujimoto, Y. et al. Surgery for Hepatocellular Carcinoma in Patients with Child–Pugh B Cirrhosis: Hepatic Resection Versus Living Donor Liver Transplantation. World J Surg 42, 2606–2616 (2018). https://doi.org/10.1007/s00268-018-4493-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00268-018-4493-1

Search

Navigation